The discovery of new reproductive material, including isolated flowers
and carpels of Axelrodia burgeri Cornet (the female inflorescence of Sanmiguelia
lewisii Brown) at the Sunday Canyon locality in Texas, provides documentation for an
apocarpous angiosperm-like flower with closed carpels and a differentiated perianth. An
isolated 14 mm long carpel compression was dissected and analyzed. It possessed an outer
thick cuticle with numerous hair bases and scattered stomata, an inner thin ovary wall
cuticle with abundant stomata, a pair of small (1 mm) basal ovules, one positioned on
either side of a closed ventral suture, and a pair of scale-like organs (adnate to the
ovary wall and possessing pollen-tube transmission-tissue characteristics) that flanked
the ventral suture and connected stigma with ovules. Resin-like beads reside within the
carpel wall, and two or three large glands' are positioned near an apical stigma. Evidence
from a silicified anatropous ovule and ovule compression suggests the presence of two
integuments. The development of carpel and ovules/seeds is graphed and compared to
patterns of comparable organ development for Magnolia spp., a monocot, and an
outgroup conifer. Axelrodia and the angiosperms all show, in contrast to the
conifer an initial delay in ovule growth until the carpels reach a similar relative size
on the growth curve, indicating that fertilization was probably required in Sanmiguelia
before the ovules continued development, an interpretation supported by the morphology
of mature seeds with embryo casts. Solitary male flower-like units of Synangispadixis
tidwelli Cornet (the male inflorescence of Sanmiguelia) and female flower-like
units of Axelrodia are homologized with male and female flower-like units belonging
to unisexual inflorescences of an associated gnetalean-like plant, reducing the
morphological gap between the Gnetales and Angiospermae. The male flower-like units of Sanmiguelia,
which bear hundreds of spirally-arranged paired biloculate anthers on the outside of a
tubular or false axis, are homologized with the carpels of Axelrodia, providing
support for the classical theory that the angiosperm laminar stamen is in fact a carpel
homologue, but that a single pair of anthers is the product of reduction. The variable
position of angiosperm anthers on the stamen is attributed to a primitive cylindrical and
fleshy filament as in Chloranthus. Direct and indirect evidence is presented for
pollination by phytophagous insects. Sanmiguelia is interpreted as a very primitive
angiosperm (i.e. taxonomically above the level of Class) that combined both monocot and
dicot characters.

Introduction

For a period of thirty years published descriptions of Sanmiguelia
lewisii Brown remained at a coarse vegetative level (Brown, 1956; Arnold, 1963; Bock,
1969; Ash, 1976; Tidwell et al., 1977) with little information on reproductive
structures except possible associated seeds (Becker, 1972). However, the discovery of a
colony of Sanmiguelia preserved in growth position with associated well-preserved
reproductive structures in northwestern Texas changed the nature of the controversy about
this Late Triassic plant (Cornet, 1986; Crane, 1988). For the first time paleobotanists could
focus on critical vegetative, anatomical, and reproductive characters in order to assess
its taxonomic affinities and phylogenetic position. Crane (1988: p. 779), in his review of
Cornet (1986),
states, 'Although [he] provides bold interpretations of these features, the evidence is
not uniformly strong [the reproductive organs] are obviously complex structures but have
so far yielded very few unequivocal points of reference from which their structure can be
interpreted with reasonable certainty.... and better preserved material may be needed to
adequately test Cornet's initial interpretations.' This paper describes or references all
of the known reproductive material, including new specimens, some of which are more
complete and better perserved than those available to Cornet (1986).
Critical aspects of Sanmiguelia'smorphology pertaining to reproductive
biology and affinity are addressed here. The author suggests that Cornet (1986) be read
for a more complete understanding of Sanmiguelia'svegetative morphology and
anatomy, and for a justification of terminology.

S. lewisii was a semiaquatic woody herbaceous plant that
resembled extant Veratrum (Liliaceae) in form and stature, but which produced a
series of clustered innovations of a few years' duration along a spreading rhizome (Cornet, 1986).
Its rhizomatous habit, vesselless secondary xylem of restricted development in the lower
part of the stem, vessels in the secondary xylem of roots, and a dicotyledonous embryo
(Cornet, 1986) are characters shared with extant Sarcandra (Chloranthaceae:
Carlquist, 1987). Its large plicate leaves had clasping or sheathing bases, four orders of
parallel venation, cross veins, and apical vein fusion, giving them a distinctive
monocot-like construction. Its unisexual reproductive structures were dimorphic as in Hedyosmum
(Chloranthaceae: Endress, 1987). The male inflorescence was a simple spike, while the
female inflorescence was a large panicle (Cornet, 1986)
that resembled the inflorescence of extant Yucca with its elongate basal axis and
apical compound branching. Large apocarpous flowers with an elaborate perianth were borne
by the female inflorescence (Cornet, 1986), while the male flowers were simple and naked (i.e.
without perianth). These combinations of characters distinguish Sanmiguelia from
any known group of gymnosperms (Crane, 1988).

Geologic occurrence and age

The Sanmiguelia specimens described here were found near the top
of the Trujillo Formation of the Dockum Group of northwest Texas (Cornet, 1986: text-fig.
1). All specimens of Sanmiguelia come from one locality along a dirt road winding
down the north wall of Sunday Canyon, just west of Palo Duro Canyon state Park, Texas. The
strata containing Sanmiguelia occurjust below a sequence of conglomerate
and sandstone, and appear to represent a shallowing upwards interdistributary lake deposit
on top of a paleosol. The Sanmiguelia colony is restricted to the west end (i.e.
shoreline) of a long gray mudstone lens, which is terminated westward by a down-cutting
sequence of channel sandstone with conglomerate lag at its base. The lacustrine clam
shrimp, Cyzicus sp., can be found in some of the dark gray shale interbeds within
the lake sequence.

The remains of Sanmiguelia lewisii were found both in growth
position and as fallen axes bearing leaves along bedding planes (Cornet, 1986).
The vertical axes were perserved as pith casts surrounded either by carbonaceous residue
or petrified wood. Except for small plicate leaves typical of Sanmiguelia on the
lower part of the stem (Tidwell et al., 1977), most of the large leaves which
characterize the plant had apparently been torn off during burial, leaving only their
sheathing leaf bases intact. Attached leaves and leaf fragments in the surrounding
siltstone were usually tattered and twisted, reflecting damage during burial. Most of the
unisexual inflorescences were found just above the paleosol in which the vertical axes
were rooted, and appear to have been knocked down and buried at times of rapid
sedimentation
(Cornet, 1986). A large apocarpous flower or fruit containing seeds (Nemececkigone
fabaforma Cornet) was found caught (preserved) between the nested rachises of Cladophlebis
macrophylla fronds, which radiated outwards from a common rhizome, indicating not only
that the fern grew alongside Sanmiguelia, but that it was probably situated
directly below an inflorescence at the time the fruit dropped.

Palynoflorules from the matrix containing Sanmiguelia and from
nearby shales at the locality are identical to those described by Dunay and Fisher
(1979) from the upper Dockum Group, and indicate a late Carnian age (Fisher and Dunay,
1984). Dunay and Fisher's (1979) study includes a palynoflorule (7A) from the same
locality. Pollen taxa diagnostic for the Late Triassic (Carnian) from the Sanmiguelia locality
are listed below. lllustrated taxa are indicated by figure references:

New specimens of Sanmiguelia (including Axelrodia and Synangispadixis)
were discovered on a field trip to Sunday Canyon in September of 1986. The new
specimens of reproductive organs are deposited at the Field Museum of Natural History,
Chicago, and include:

Some specimens required degaging in order to reveal hidden parts (Fig.
4). Most specimens, however, provided enough evidence for study and interpretation without
any significant preparation. A transfer peel using cellulose acetate film was made of a
cluster of well-preserved flower-like units (Figs 3-4). JOEL and lSI-40 SEMs were used
(during different periods) to study individual anthers and transfer preparations of large
fragments of male flowers (Figs 10-12), and a petrified ovule recovered from one partly
silicified carpel (Fig. 3). The samples were sputter coated with less than 250 angstroms
of gold. A Tracor Northern energy dispersing spectrometer was used in conjunction with the
ISI-40 to detect illite clay inside the ovary of one carpel compression. Portions of male
flowers were embedded in plastic, sectioned, and polished. Sections were studied and
photographed using a Zeiss reflectance microscope. Standard palynological techniques were
used to secure pollen masses, individual pollen grains, and outer cuticle from anthers
(Fig. 13), as well as cuticle, transmission tissue, and portions of an ovule from one
carpel compression (Figs 5-6). Preparations of pollen and cuticle were studied using a
Zeiss binocular microscope and photographed with a Zeiss photomicroscope containing
built-in camera. Photographs of the megafossils were made using a Minolta 35 mm camera
with enlargement lenses.

Morphological development of Axelrodia carpels was compared with
that of Magnolia grandiflora, M. virginiana (Magnoliaceae), Serenoa repens (Arecaceae),
and an outgroup conifer, Thuja orientalis. The recent plant specimens were
collected during the spring and early summer of 1987 at five-seven day intervals from
plants growing in the Houston, Texas area. Megasporophyll length versus two dimensional
area and ovule/seed size in mm2 were plotted for Axelrodia, while carpel length
versus carpel and ovule/seed weight in milligrams were plotted for the angiosperms. Cone
length versus cone and ovule/seed weight in milligrams were plotted for Thuja, because
dissection of individual ovule-scale units caused irregular damage and excess fluid loss,
and because the scales of one cone differed significantly in size. Weights were obtained
on fresh material and on specimens preserved in alcohol using an electronic balance
sensitive to 0.001 milligrams at GeoChem Labs. Inc., Houston, TX. Multiple readings were
taken until relatively stable (plateau) measurements were obtained due to initial weight
loss from evaporating liquids.

Previous interpretation (Cornet, 1986)

The male and female reproductive structures of S. lewisii were
borne on separate inflorescences. The female or ovuliferous inflorescence was named Axelrodia
burgeri, while the male or polliniferous inflorescence was named Synangispadixis
tidwellii. Axelrodia resembled a typical monocot inflorescence (sensu Lilium or
Yucca) with its elongate central axis bearing clasping bracts basally that
elongated apically to sheathing cataphylls. It undoubtedly terminated a main vegetative
axis because of its large size (over 48 cm in length). Secondary branches arose from the
axils of cataphylls, possessed numerous spirally-arranged scale bracts, and bore two types
of flower-like structures (Figs 1-2): (1) Solitary ovuliferous units consisting of a
central megasporophyll (carpel) surrounded by two types of bracts, one peltate and hairy
and the other elongate, digitate, and glabrous. Solitary units were each subtended by an
elongate conduplicate bract, and they were clustered together in twos or threes along the
secondary branches on short tertiary shoots (Fig. la); (2) Large composite flower-like
units terminated the secondary branches (Fig. la). Cornet (1986) compared this composite
unit to an apocarpous angiosperm flower, because it possessed numerous carpel-like
megasporophylls centrally borne on a receptacle, which was subtended by at least two
whorls of modified bracts (compare Figs la and 2c).

Synangispadixis resembled an aroid inflorescence (sensu
Arisaema) in which naked synangia-like units (Fig. 2a) were spirally borne on an
elongate central axis (over 24 cm in length) that probably terminated the main vegetative
axis. Synangia-like units were also described as being attached in clusters at the ends of
secondary vegetative branches, which bore parallel-veined leaf-like bracts that decreased
in size apically down to scale bracts with three veins. Each synangia-like unit bore
hundreds of sessile, paired biloculate rnicrosporophylls (Fig. lb). Evidence was
presented that indicated enlargement and longation of these units at anthesis.

Axelrodia and Synangispadixis were probably subtended by a
large spathe-like vegetative leaf, marking an abrupt transition from vegetative to
reproductive axis. Since neither inflorescence was found organically attached to a
vegetative axis, even though male synangia-like units were found at the ends of secondary
vegetative branches, Cornet (1986) could not determine if Sanmiguelia was
monoecious or dioecious. A monoecious habit was implied by the location of fallen male and
female inflorescences, which were found lying adjacent to the same cluster of rooted
vertical axes.

The megasporophylls were described as carpel-like, with a tapering base,
which expanded upwards to a rounded apex and terminated in a bilobed U-shaped stigma-like
collar encircling a small canal or opening into a hollow chamber or ovary (Fig. 2b). The
megasporophylls were covered with long multicellular and glandular hairs. Two
shoulder-like bulges flanked the apex of immature megasporophylls, but became much less
prominent on larger megasporophylls.

The microsporophylls were described as anther-like, double-walled with a
constricted base, but without filament (sessile). They were borne in symmetrically opposed
pairs, and these pairs were arranged in a tight spiral around immature secondary axes
(Fig. lb). The paired (biloculate) pollen masses were surrounded by remnants of a tapetum,
and the septum separating them largely disappeared at maturity, producing one united
pollen chamber containing hundreds of small, elliptical, psilate tectate-granular
monosulcate pollen.

Results and revised descriptions

Cornet's (1986) interpretation of Sanmiguelia's reproductive
structures was based on a small number of specimens, and therefore suffered from a lack of
adequate sampling, but also from the coarse screen size (resolution) of the photographic
plates. Those problems are largely corrected with the data described and illustrated
below. Inaddition, some of the previous interpretations were based on a poor
understanding of homologous structures. The terms, carpel-like and anther-like in Cornet
(1986), are replaced by carpel and anther, respectively, for simplicity of expression, and
because their morphology and structure are now well-enough known (see below and Cornet,
1986) to infer homology. As in any fossil material, the assignment of homology is an
hypothesis.

The study of additional specimens (the subject of this report) and their
comparison with associated gnetalean-like reproductive structure (Cornet, 1987a and b) has
shown, for example, that the synangia-like secondary branches are in fact solitary
flower-like polliniferous units (i.e. male 'flowers'), which are homologues of the
solitary flower-like ovuliferous units (compare figs 2a, 2b apd 7a-d): The homology is not
at first obvious, because the male and female units are so different in outward
appearance, but this homology is all important in understanding how the A.xelrodia carpel
evolved and its bearing on angiosperm and parallel gnetalean evolution.

The basic organization and structure of the inflorescences (i.e. Axelrodia
and Synangispadixis) have not changed with the study of new specimens. The new
specimens support Cornet's (1986) original descriptions, and provide additional
documentation for the construction of male and female 'flowers' (the term 'flower' is put
in quotes to distinguish solitary ovuliferous and polliniferous units from compound
apocarpous flowers borne at the ends of secondary branches). For example, the discovery
and study of an isolated megasporophyll compression (Figs 3b, 5a-b) provide support for
its carpel-like construction. The discovery of additional solitary ovuliferous units (Fig.
3f) confirms bract morphology as described for the original specimens (Fig.4a-e).
Moreover, a partly silicified carpel yielded upon transfer preparation an immature
(presumably unfertilized) petrified ovule that shows critical morphological characters
(Fig. 3e).

Axelrodia burgeri Cornet

An exceptionally well-displayed specimen of a pre-Cretaceous
angiosperm-like flower is illustrated in Figure 3c. It was borne at the end of a secondary
branch on an inflorescence, and shows a central gynoecium (gy) comprised of numerous
carpels attached to the upper part of a receptacle (an isolated carpel is provided in Fig.
3b for comparison). Portion of the secondary branch (2br) is still attached and bears at
least one scale bract (sb). Attached to the lower part of the receptacle are hairy and
digitate bracts (hb and db); which are subtended by four conduplicate bracts (cbl-4). One
conduplicate bract (cbl) disappears beneath the gynoecium, and its base emerges in a
window in the region of the receptacle (white double-headed arrow). Unfortunately this
specimen was discovered in a pile of rubble from excavation, and its counterpart was not
recovered. Consequently, the number of carpels cannot be determined as in the
three-dimensionally preserved gynoecium (Fig. 4a-c). A fragment of Sanmiguelia leaf
is also present, which shows at least two orders of parallel venation.

The conduplicate bract is so named because it possessed a strong central
keel and V-shaped form that typically caused it to fold in half upon burial. Three of the
basal conduplicate bracts in Figure 3c are preserved folded and therefore appear half
their normal width. One bract (cb4), however, was rotated upon burial so that it was
spread open with its keel prominently displayed as if it were a median vein. Cornet (1986)
was able to recognize the morphology of this bract from two specimens (Fig. 4d-e), because
sediment was present between the folded halves.

The morphology of hairy peltate and glabrous digitate bracts was not
adequately illustrated and documented by Cornet (1986), although their existence was clear
to him from the study of specimens in Figure 4 (a-e). The distinction was obvious due to
the presence or absence of cuticular hairs and the digitate versus peltate morphology of
the bracts. Figure 3f illustrates a transfer preparation of partly dismembered solitary
ovuliferous units or female 'flowers', and again shows the presence of both bract types
(db and hb). The peltate hairy bract can be seen more clearly than in other specimens,
while the narrow straps with central veins of possibly two digitate bracts merge and unite
towards a probable juncture with a carpel (cp on left: partly silicified and incomplete).
In addition, there are unusual filament-like structures associated with and attached to
the digitate bracts (open arrows), which are shown in Figure 2b.

The morphology of the secondary branches of Axelrodia was not
adequately illustrated by Cornet (1986), mainly because only portions of them were visible
on the type specimen. The transfer preparation in Figure 3f shows a secondary branch (2br)
c1osely associated with two solitary ovuliferous units, and although it is complete
between part and counterpart (double-headed arrow), organic connection with the
ovuliferous units is not apparent. There is an indication, however, of a possible branch
(3br?) connection between the carpel to the right (cp) and the secondary branch.
Furthermore, numerous scale bracts are visible on the secondary branch, giving it the
appearance of a Pagiophyllum conifer shoot.

The Axelrodiacarpel

Cornet (1986) provided evidence that the Axelrodia carpel was
originally hollow when he identified a sediment-filled megasporophyll containing possible
cross sections of ovules in a three-dimensionally preserved gynoecium (Fig. 4a-c). Since
there was only one example that clearly showed these features (other evidence was more
circumstantial: e.g. paired seeds within a carpel: Fig. 4a), comparison with angiosperms
lacked strength. The isolated carpel compression illustrated in Figure 5a:-b, however,
perserves some of the most critical evidence for the homology of its structure with an
angiosperm carpel, as well as some unexpected evidence for biotic pollination.

Axelrodia carpels range in form from inverted bell-shaped (Figs
3f and 4h) to egg-shaped (Figs 3a and 4g). A stigma-like apex is present on all carpels,
but is sometimes spread apart on the bell-shaped form probably due to distortion during
compression (Fig. 4h). Two gland-like swellings create shoulders or pronounced appendages
distally (g), and appear to be symmetrically (bilaterally?) positioned on opposite sides
where the carpel begins to taper towards the stigma-like apex. These swellings are more
pronounced on the inverted bell-shaped form (Fig. 4h), leading Cornet (1986) to speculate
that their development anticipated the enlargement of the ovary to accommodate developing
seeds. The new specimens (Figs 3f and 4g) indicate, however, that differences in form may
be related to the degree of gland development, because the more carpel-like form (Figs 4g
and 5a-b) appears to owe its shape to three small glands (evidenced by ovoid organic
stains in the matrix under the glands) distributed across the dorsal side instead of two
large glands (Fig. 4h).

Evidence for a carpel wall

Oxidation and clearing of pieces of a carpel compression in a basic
solution (Fig. 5a-b) yielded several different types of tissue or cuticle. The most
obvious cuticle is from the outer wall, which is thicker than the inner cuticle, possesses
well-defined rectilinear cell outlines and a fine tread-like pattern (Figs 5c, 6a, 6f and
6h), and reveals the circular to elliptical bases of hairs (b), which are usually situated
within the boundaries of epidermal cells. When hairs are recovered in cuticle
preparations, they are usually long, thick-walled, and sometimes aggregated (Fig. 5e)
rather than widely spaced as the distribution of hair bases would suggest. There are also
narrow lens-shaped structures with a prominent median thickening, which may represent
either stomata or glands (s). Pollen can be found adhering to the outer cuticle; the most
common type is monosulcate like that of Synangispadixis (Fig. 6a and 6f., arrows),
but other types are also present, such as Patinasporites densus (compare Fig. 6h
and 6i). The inner wall cuticle, however, is much thinner, tends to fold rather than
break, and possesses in some areas numerous closely-spaced stomata (Fig. 5d). The greater
abundance of stomata inside the ovary wall may be related to humidity control in a
semi-arid climate or to fluid volume control within the ovary. A secretion or
mucilage, typically fills the ovary in the Chloranthaceae (Endress, 1987a) and Araceae
(personal observation). Stomata on both inner and outer carpel-wall cuticles support a
leaf origin.

Evidence for a pollen tube transmission tissue

A third type of tissue or organ is preserved between the cuticles of the
dorsal and ventral walls. It can be demonstrated in pieces of compression viewed in cross
section under SEM (Fig. 10c-d). A middle layer (t in Fig. 10d) can be seen to originate
and thicken from left to right in Figure 10c. This layer is attached or appressed to the
ventral wall (v) and separated by a thin layer of illite clay (SEM elemental spot
analysis) from the dorsal wall (d). The clay occupies what volume remains of the collapsed
ovary cavity, and probably entered the ovary at the time of burial (cf. Cornet, 1986). The
position of the middle layer on the ventral side of the carpel was determined by observing
the position of the white clay layer (obvious against the coal-black compression) in place
on the specimen (Fig. 5a-b), and its relationship to the side of the compression
containing the impression of the ventral suture. The distribution of the middle layer (t)
was followed through the compression (possible because of the distribution of compression
fragments: Fig. 5a-b) and plotted. It is shown in Figure 9a as the area with the diagonal
pattern. It clearly straddles the ventral suture and extends from near the stigma-like
carpel apex basally to include the area occupied by two ovules (Fig. 5a, o), one on either
side of the ventral suture (Fig. 9a). The ovules were identified as an additional layer by
their size and ovoid shape within the compression, and by oxidizing and clearing a piece
of one of them (Fig. 6d and 6g).

The middle layer (t), when isolated, oxidized and cleared, has a very
distinctive fibrous structure or texture (Figs 5g and 6d). Beads of resin-like material
were found situated between the middle layer and the ventral wall (Fig. 6e), and also
adhering to or within the middle layer (Fig. 6d). The distribution of this layer down to
the ovules is documented in Figure 6d and 6g, which show this layer in contact with the
thick compression of multiple cuticles belonging to one ovule. The exposed surface of the
middle layer facing the ovary cavity was visible in one compression fragment under SEM
(Fig. 5t). Its surface is covered by thousands of minute papillae arranged in rows. The
rows give the middle layer its fiber-like texture. They are oriented vertically or
baso-apically within the carpel; their orienation was determined by the orientation of the
compression fragment in Figure 5f, which is located by the x in Figure 5a.

The middle layer appears to be divided by the ventral groove into two
bilaterally-symmetrical elongate scale-like organs which were appressed to the ventral
wall and extended from the area of ovule placentation apically to the base of the stigma
(Fig.9a-b). The papillate character of their outer surface, the orientation of those
papillae in vertical rows aligning stigma with ovules, and the distinction of this layer
from any ovular integument (or micropyle) by direct comparison (Fig. 6d and 6g) strongly
suggest that these paired organs functioned as a pollen tube transmission tissue. The
presence of resin-like material within the middle layer and ventral wall (Fig. 6d-e)
suggests the production of a non-polar terpenoid resin that probably had toxic properties
when fresh and fluid, and may have been a defense against attack by pathogens, herbivores
or seed predators (Armbruster, 1984). There is no indication of pollen either within the
ovary or clinging to the side of the middle layer facing the ovary. No pollen was found
trapped between the cuticles of the middle layer, which would probably have occurred if
the transmission tissue contained fluid-filled passages or channels connecting mouth
and micropyles as in Caytonia and Glossopteris (Reymanowna, 1973; Gould and
Delevoryas, 1977; Crane, 1985). A polar fluid containing polysaccharides and carbohydrates
for pollen tube growth is unlikely to survive fossilization, while resin-like material
within the middle layer probably would survive fossilization. The similarity of the
massive middle layer to the more massive types of transmission tissue possessed by the
Chloranthaceae (e.g. Hedyosmum mexicanum and Ascarina lucida: Endress,
1987a) and some Araceae (e.g. Anthurium, personal observation) is consistent with
the low phylogenetic position suggested for the Chloranthaceae and Arales (Endress et
al., 1987a; Dahlgren et al., 1985).

The presence of transmission tissue on the outer surface of Axelrodia
stigmas has not been verified, although a modified cuticle does exist there (Cornet,
1986: p. 260). The mapped termination of the middle layer just before reaching the stigma
(Fig. 9a) may be an error due to the inability to follow this layer below a certain
thickness. Transmission tissue exudate (cf. Cresti et al., 1986; Endress, 1987a)
may have filled the short stylar canal and wetted the stigmatic surface, thereby bridging
any gap between pollen landing surface and transmission tissue in Axelrodia. Conversely,
an abscence of the middle layer from the stigma may be a primitive characteristic, which
correlates with a psilate pollen grain lacking a porous exine structure indicative of a
sporophytic incompatibility mechanism (Zavada, 1984; Zavada and Taylor, 1986). Sporophytic
self-incompatibility requires (1) physical contact between a porous pollen exine and
transmission tissue so that sporophytic substances produced by the anther tapetum and
carried by the exine can influence the gametophytic system directly (Zavada, 1984), and
(2) chemical agents produced by the tapetum that will influence compatibility.
Consequently, a sporophytic incompatibility mechanism and a porous exine (i.e.
reticulate-columellate) probably evolved after transmission tissue formed its own stigma
or stigmatic surface above the carpel as in Hedyosmum, Ascarina, Chloranthus, etc.
(Endress, 1987a).

Evidence for bitegmic ovules

Pieces of an ovule recovered from the carpel compression in Figure
5a-b are comprised of numerous layers of thin cuticle, so many in fact that oxidation and
clearing could not make them transparent (Fig. 6g). Although the exact number could not be
determined, the layered edges of broken ovular compression suggest as many as ten
cuticles in cross section, more than can be accounted for by a unitegmic ovule with
enclosed nucellus.

Fig. 6. A-I. New gnitalean like 'flowers' belonging to
urusexual inflorescences or spikes from the Sanmiguelia locality. A. Distal end
of female spike showing apical compression of two 'flowers' (arrows pointing to ventral
sutures: vs), and lateral compression of several other 'flowers'; a ring of interseminal
scales (numbered) is visible in the apical compressions; scale in mm. B. Bell-shaped apex
of a female 'flower' showing ventral suture (vs at arrow) spread open, gland-like
structures (small arrows) around rim of cupule, and tops of enclosed interseminal scales
(ts at arrows) forming a carbonaceous 'bridge' across cupule; scale X4. C. Isolated seed
cast; scale in mm. D. Two trumpet-shaped female 'flowers' attached to spike axis; apices
to 'flowers' incomplete; small gland-like-structures on tubular part of cupule visible at
arrows; scale in mm. E. Lateral compression of female 'flower' showing interseminal scales
separated by matrix on one side of cupule, sediment fIlling space once occupied by a seed,
small gland-like structures on tubular part of cupule (small arrow), position of ventral
suture (vs), and a possible non-functional ovule (ov?) at base of cupule replaced by
siderite; scale X6.2. F. Base of a female 'flower' showing sediment cast of seed (sd) and
a small lobate bract attached to base of cupuIe; scale in mm. G. Portions of four male
'flowers' compressed baso-apically and showing crowded bivalved microsporophylls attached
to outside of cupule; fiber-like structures or hairs visible within one cupule (arrows);
scale X3. H. Cross sections of two male 'flowers' showing tubular base and bell-shaped
apex; most of the bivalved microsporophylls pulled off during burial and are 'floating' in
matrix between 'flowers'; note tattered margins of cupule and presence of some
microsporophyll bases on inside of rim to cupule (arrows); scale X4. I. Bell-shaped apex
to a male 'flower' showing bivalved microsporophylls attached to rim of cupule (a pair of
bracts to one microsporophyll at arrows); scale in mm.

The most convincing evidence for two integuments comes from a
silicified ovule (Fig. 3e), recovered during the transfer of solitary 'flowers' to
cellulose acetate film (Fig. 3t). The ovule is about 1.0 mm long. A distinctive recurved
funicle or raphe (i.e. ridge) can be identified, substantiating an anatropous condition,
and a large micropyle (Fig. 3e, m) can be seen at one end adjacent to the hilum (Fig. 3e,
h). An inner integument forms the border of the micropyle, while the distal end of the
outer integument can be recognized by its raised margin (Fig. 3e, arrow). Normally the
outer integument of angiosperms extends beyond the inner one. Ovules with a prominent
inner integument, which projects well beyond the outer, are occasional, as in the
Chloranthaceae (e.g. Chloranthus, Hedyosmum), Annonaceae, Trapaceae, Proteaceae,
and some of the Cactaceae (Ean1es, 1961; Endress, 1987a). This specimen compares in size
and morphology with an unfertilized, anatropous, bitegmic angiosperm ovule.

Evidence for biotic pollination

The carpel compression illustrated in Figure 5a-b is preserved as both
part and counterpart, but it is badly cracked and divided between the two halves. The
manner of preservation allows both sides to be observed as impressions in the matrix.
Figure 9a gives locations of pieces of cuticle and ovular integument removed for scanning
electron microscopy (SEM) or for transmitted light microscopy (SLD). The matrix impression
contains organs and structures that were attached or adhering to the outer cuticle. The
position of the ventral suture can be followed from the cleft stigma basally as a groove
or crease to the position of the ovules (compare Figs 5a, arrows, and 9a). Its arcuate
shape is probably due to the collapse of the ovary. A similar groove or indentation
marking the position of the ventral suture can be seen in a carpel cross section (Fig. 4b,
above arrow). In addition to a few epidermal hairs embedded in the matrix (most hairs are
missing or preserved only as hair bases on the outer cuticle: Figs 5c, 6a and 6t), there
are fragments of cuticle from the edges of tears in the carpel wall (FIg. 5b-c, arrows),
and fragments of Synangispadixis anthers (Fig. 9a, black and white tear-drop shaped
objects; the black fragments are on the ventral side, the white ones on the dorsal side).

Most of the anther fragments are the distinctive thick-walled borders to
the distal suture (e.g. Fig. 10a-b), and may have been transported to the carpel as the
indigestible portions of an insect's meal. The tears in the carpel wall have a distinctive
arcuate shape suggestive of cuts that could have been made by a chewing insect's
mandibles. Most of the cuts are on the dorsal side of the carpel, which had a thinner wall
(Fig: 8b), while most of the anther fragments are aligned in a row on the ventral side as
if deposited along an insect's path. The presence of resin-like material between the
cuticles of the carpel wall, and the presence of large specialized glands situated near
the stigma suggest the presence of both a pollinator reward system (i.e. nectar or
nutrient) and a defense system (i.e. antibacterial, fungicidal, and antiherbivor toxins:
Armbruster, 1984). Finally, the carpel was physically or physiologically severed from its
'flower', and the jagged edge also could have been caused by the chewing action of an
insect. If phytophagous insects were the primary pollinating vector, perhaps the formation
of a terminal apocarpous flower is an evolutionary response to counteract the attacks on
solitary ovuliferous units.

Floral phyllotaxis of the compound apocarpous flower

The organization of floral organs is similar between solitary
ovuliferous units borne on tertiary branches and the large apocarpous flower borne at the
ends of secondary branches (Fig. la), with each organ type maintaining the same relative
position in the floral structure even though tire number of parts increased
disproportionately in the apocarpous flower. Whereas the solitary 'flowers' had one
carpel, one conduplicate bract, and probably two hairy and two glabrous bracts, the
apocarpous flower had from few to many carpels subtended and surrounded by an
indeterminate number of hairy and glabrous bracts, which were themselves subtended by a
pseudowhorl or whorl of four elongate conduplicate bracts. An ordered arrangement of
carpels is not apparent from the study of a three-dimensionally preserved gynoecium
(Fig. 4a-c), and the reconstruction in Figure 2c suggests that not all carpels were
oriented anteriorly, possibly indicating an origin from more than one floral primordium.
Conversely, variable orientation of carpels may be a primitive character, since it also
occurs in the Chloranthaceae (Endress, 1987a).

Angiosperm flowers with a small number of perianth parts typically have
gynoecia with few carpels which are usually whorled or fused (Endress, 1987b). Unisexual
female flowers of some Alismataceae and Ranunculaceae are an exception. In these flowers a
large apocarpous gynoecium probably evolved from an increase in number of carpel initials
(Dahlgren et al., 1986). Axelrodia apocarpous flowers show a decrease in
number of parts basally for each organ type, allowing for a more ordered arrangement
basally (cf. Endress, 1987b). The origin of a poorly organized gynoecium with a variable
number of carpels may be related as much to extrinsic factors (e.g. the type and
effectiveness of biological pollinators) as to intrinsic ones (e.g. an origin from the
condensation of numerous floral primordia). The presence of both solitary and compound
floral types in Sanmiguelia may be the first clear evidence that the polycarpous
angiosperm flower (and its derivatives) is not directly homologous with gnetalean and
bennettitalean 'flowers'. The simple flowers of the Chloranthaceae (Endress, 1987a) and
Piperales may be the exception (Burger, 1977).

Origin of a closed carpel

At the Sunday Canyon locality isolated leaves of Pelourdea poleoensis
were found in the paleosol underlying the Sanmiguelia root zone and in thin
shales interbedded within the sandstone sequence overlying the Sanmiguelia colony.
The leaves of both taxa are frequently reported from the same localities (Ash, 1987a).
Both plants had an herbaceous habit, grew to a similar overall size, possessed large
leaves with parallel venation and clasping leaf bases, and lived in the same habitat (Ash,
1987a, 1987b), suggesting a close ancestral relationship. Five unisexual reproductive axes
or inflorescences bearing gnetalean-like 'flowers' were found in the paleosol just below
the Sanmiguelia colony (cf. Cornet, 1986), while an additional one was found within
the clayey siltstone beds entombing the Sanmiguelia colony (Fig. 8a-i: Cornet,
1987a; In Prep.) They are all spikes possessing a thick central axis with a large pith
cast, like that of Pelourdea and Sanmiguelia (Ash, 1987b; Cornet, 1986).
Four long male spikes were found in a block of siltstone next to a large axis and long
lanceolate leaf of P. poleoensis. They are oriented in the same direction as if
attached to a common axis, but the adjacent block which would show an organic connection
was mistakenly not collected. The scarcity of Sanmiguelia leaves in the paleosol,
organic connection between Synangispadixis and Sanmiguelia, and the
association of Axelrodia with a large leaf of Sanmiguelia (Cornet, 1986)
indicate that the new reproductive structures do not belong to Sanmiguelia. They
probably belong to Pelourdea, based in part on the large number of vegetative
parallels between Pelourdea and Sanmiguelia, in part on additional parallels
between Axelrodia, Synangispadixis, and the new reproductive structures (described
below), and in part by the process of elimination, since no other 'autochthonous' seed
plants have been identified in the Sanmiguelia facies zone.

The gnetalean-like 'flowers' of the new inflorescences are remarkably
similar in form to the inverted bell-shaped variation of the Axelrodia carpel
(compare Figs 7b and 7d; 4h and 8d, e), warranting a more detailed description and
comparison: male or female 'bisporangiate' inflorescences, at least 13 cm in length and
differing mainly in the functional development of either ovules or pollen sacs, bear up to
one hundred, 1.5 cm long, spirally-arranged tubular trumpet-shaped 'flowers' with
multitier lobate margins (Figs 7c-d; 8a-i). Each trumpet-shaped 'flower' has a ventral or
anterior suture which is frequently 'open' or spread apart at the bell-shaped apex (Fig.
8a and b, vs at arrows), but usually closed along the floral tube (Figs 7c-d, 8e, vs).
Attached to the outside of the male 'flower' (Fig. 7c) are hundreds of bivalved
microsporophylls (Figs 8g-i), each with a central elongate pollen sac or hollow stalk that
divides apically into a cluster of 4-6 small sacs, which contain small (18-25 um), oval,
psilate monosulcate pollen. Microsporophyll construction is very different from
that of Synangispadixis, but very similar to that of Ephedra. InSynangispadixis
the paired bract homologues are each apparently folded to enclose a pair of pollen
sacs (creating the tetraloculate condition in angiosperms), while in the new plant the
bracts remained free. Inside the narrow tubular base of the gnetalean-like male 'flower'
is a cluster of thick fibers or hairs (Fig. 8g, arrows).

Inside the gnetalean-like female 'flower' (Figs 7d; 8d) a single central
ovule with a long narrow apex (Figs. 8c; 8f, sd) was surrounded by a ring of about six
sterile scales (Fig. 8a, e). These scales, which are reminiscent of the interseminal
scales of the Bennettitales, rise to the top of the tubular part of the cupule (Fig. 8b,
ts),where they form slightly expanded heads at the base of the inverted-bell-shaped floral
apex (Fig. 8a, numbered in one of two apical views indicated by arrows). The apex of
the seed (micropyle?) appears to extend to near the top of the surrounding scales.
Possible aborted or non-functional ovules occur next to the central ovule or
sediment-filled cavity at the base of some cupules (Fig. 8e, ov?). Along the lower part of
the female 'flower' possibly four or five lanceolate to semi-digitate scale bracts insert
around th4 floral tube (Fig. 8f, br) below small gland-like structures (Figs. 8d and e,
small arrows). These gland-like structures may represent sterile microsporophyll
homologues, based on an attachment identical to the microsporophylls of male 'flowers'.
They increase in number and size around the cup-shaped apex of the female 'flower',
forming a dense cluster of ovoid bodies supported by narrow filaments (Figs 7d; 8b, small
arrows).

Fig. 7. A-D. Reconstructions of angiosperm and
gnetalean 'flowers' from the Sanmiguelia locality. A. Synangispadixis tidwellii male
'flower' showing a lack of perianth, and crowded paired microsporophylls attached to the
outside of an apically constricted or closed, tubular (i.e. cupulate) floral axis. B.
Axelrodia burgeri female 'flower' showing two types of perianth bracts, an
associated glandular organ (Fig. 7b) which was probably attached to a digitate
bract, and a cupulate structure (i.e. carpel). with subapical glands, a
constricted apex with ventral suture forming a stigma, and a pair of subbasal
anatropous bitegmic ovules enclosed within an ovary. C. Gnetalean male 'flower' showing
a lack of perianth, a ventral suture, and crowded bivalved microsporophylls attached
to the outside of a cupulate structure. D. Gnetalean female 'flower' showing a
ventral suture, glands instead of microsporophylls attached to the outside of a cupulate
structure, ring of sterile scales surrounding cavity where a single seed developed,
and small digitate bracts forming a rudimentary perianth.

The parallel morphology between Synangispadixis and Axelrodia 'flowers',
on the one hand, and between the male and female gnetalean-like 'flowers' on the other
becomes apparent when they are compared to each other (Fig. 7a-d). Both types of male
'flowers' are naked (lacking basal bract-like appendages) and covered with
microsporophylls, while both types of female 'flowers' possess basal bract-like
appendages, gland-like organs (instead of microsporophylls) which are concentrated
apically, ventral sutures, and one versus two functional qvules attached near or at the
base of a cupulate structure. The similarity in form between some Axelrodia carpels
(e.g, Figs 3f and 4h) and the basic copstruction of the gnetalean-like male and female
'flowers' suggests a fundamental and ancestral relationship as predicted by cladistic
analyses forthe GnetaIes and angiosperms (Crane, 1985; Doyle and Donoghue, 1986,
1987a).

The origin of the closed carpel in Axelrodia can be conceived as
a parallel development between male and female 'flowers'. A false or closed tubular axis
and a constricted apex (i.e. not flared) for the Synangispadixis 'flower' (Fig. 7a)
are implied by comparison with the parallel morphology of tubular trumpet-shaped
gnetalean-like 'flowers', and to a lesser extent by its enlargement in breadth during
anthesis and the lack of a vascular core (Cornet, 1986; Figs 11a-c and 13c). Similarly,
the female Axelrodia 'flower' (Fig. 7b) has a constricted apex that forms an ovary
and creates the necessity for pollen to land and germinate on carpellary tissue. Although
the 'flowers' of Axelrodia and Synangispadixis outwardly do not appear
homologous, comparison with the associated gnetalean-like 'flowers' suggest that they are
fundamentally similar and bisexual as in extant Gnetales and the extinct Bennettitales
(Crane, 1985; Doyle and Donoghue, 1987a, 1987b).

Synangispadixis tidwellii Cornet

Two additional specimens of S. tidwellii were discovered
in 1986, and each is preserved as a compression containing murnniified anthers (Fig.
11b-c). Cornet (1986) described the male 'flowers' as secondary branches terminated by
synangia-like organs. The male 'flowers' are now recognized as probable homologues of Axelrodia
solitary ovuliferous units or female 'flowers' (compare either Figs 2a-b or 7 a-b).
The specimen illustrated in Figure 11c has an inflorescence axis that bifurcates or
branches near its end (not shown), a characteristic which was not observed by Cornet
(1986) and which reduces the morphological gap between the female inflorescence or panicle
and the male inflorescence or spike (see reconstructions in Cornet, 1986; Fig. 6). In all
specimens of S. tidwellii the 'flowers' insert spirally around the main axis, and
there are no bracts or perianth-like structures evident. The holotype (Fig. 11a) shows
acropetal maturation with mature male 'flowers' restricted to the lower part of the
inflorescence axis. Apical anthers of undehisced 'flowers' are less mature than basal
anthers (Cornet, 1986). Dehisced 'flowers' at the base of the inflorescence (Fig. 11a)
have a longer than usual, naked lower floral axis that may be the result of deciduous loss
of anthers after dehiscence.

The male 'flower' and its homology with angiosperm stamen

The homology of male and female solitary 'flowers' and their similarity
to associated gnetalean-like 'flowers' (Fig. 7c-d) suggest that the male floral axis is in
fact a closed tube or false axis. The axis, when visible, is preserved as a thin
carbonaceous layer with no apparent vascular core (Fig. 11 c), which would be expected if
it was ontogenetically 'hollow'. The possible origin of both the Axelrodia carpel
and Synangispadixis floral axis from homologous tubular or cupulate structures
gives new vitality and meaning to the classical or traditional comparison of the laminar
stamen and carpel to unfolded and folded leaves, respectively (Canright, 1952; Bailey and
Swamy, 1954; Eames, 1961). The major difference between the Synangispadixis 'flower'
and the laminar stamen is that the former posseses hundreds of paired sessile biloculate
anthers, while the latter contains only one pair. That difference, however, can be easily
rectified through reduction. Few angiosperms produce stamen with more than two anthers,
and those that do usually have no more than eight (Eames, 1961). The reduction to one pair
may be related to the timing of anthesis, which could not be synchronized or limited to a
short period of time with acrofloral anther maturation as in Synangispadixis. Investment
in one enlarged pair of anthers instead of hundreds of small ones may be a specialization
related to more selective insect pollinators, or to interspecific competition for those
pollinators.

Fig. 9. A and B. Isolated Axelrodia burgeri carpels
(Fig. 5A-B). A. Camera lucida drawing of carpel showing distribution of middle
layer (cross-hatched pattern). two ovules (clear ovoid areas within cross-hatched
pattern), ventral groove or suture, " anther fragments on dorsal side (white) and
ventral side (black) of carpel, and positions from which fragments of carpel compression
were taken to make cuticle slides (SLD) and sc1anmng electron, micrographs (SEM). Dot
pattern: one dot = only dorsal and ventral wall layers present; two dots = dorsal,
ventral; and middle layers present; three dots = dorsal, ventral, middle, and ovule layers
present; dots in position where data recorded. B. Reconstruction of carpel in A with
interpretations (see text).

Some more advanced angiosperms produce stamen bundles, which are best
known in the Guttiferae and in certain Australian genera of Myrtaceae (Stebbins, 1974).
Stamen bundles may be the only functional analogues to Synangispadixis 'flowers'
among extant angiosperms, giving an insect the illusion of a greater food or pollen source
without sacrificing anthesis timing. Based on the homology of carpel and stamen,
syncarpous gynoecia and stamen bundles in angiosperms could be homoplastic structures.

Primitive laminar stamen are recognized with either abaxial, adaxial, or
marginal anther attachment (Canright, 1952; Eames, 1961). Evolution from a tube or
cylinder allows for virtually any type of attachment. Chloranthoid androecia with
cylindrical stamen and variable anther attachment are known from the Early Cretaceous
(Friis et at., 1986). Furthermore, the presence of a ventral suture on the male
gnetalean-like 'flower' (Fig. 7c) implies that the Synangispadixis 'flower' also
possessed a closed ventral suture, giving the floral axis the genetic option of either
unfolding or flattening to produce a laminar structure, or remaining cylinder to produce
the narrow filament so common among angiosperms.

The Synangispadixis anther

Synangispadixis anthers are arranged in spiral rows around the
flora axis, and occur in opposite pairs as in angiosperms (Fig. 1b; Cornet, 1986).
The new material clearly shows this arrangement (Figs 10a, 12a, 12c). The anthers in
Figure 10a conveniently possess contrasting electron densities in different rows. The tip
to tip (t) and base to base (b) arrangement is apparent in Figure 122a and 12d, while it
is not as apparent for narrow-elongate or immature anthers with poor tip and base
(abaxial/adaxial?) differentiation (Figs 10a, 12c). The paired arrangement is not only
critical to an angiospermous affinity, but also to an ancestral relationship with sister
groups, the Gnetales and Bennettitales (Doyle and Donoghue, 1987a), for which the basic
microsporophyll construction is similar in having a distinct bivalved (paired)
construction.

Fig. 10. A and B. Synangispadixis tidwellii microsporangia
or anthers; note alternating electron density for anthers belonging to different rows on
flora axis in A; enlargement of one anther in B. Fig. 10C and D. SEM view of piece of Axelrodia
burgeri carpel compression (from specimen in Fig. 8A-B), with ventral surface up (to
the left); note decrease in thickness from right to left (from up to down) due to
disappearance of middle layer in C, and separation of dorsal wall (d) from adnate ventral
wall (v) and middle layer (t) by illite clay layer in D. Mounting glue forms threads
bridging fractures. SEM magnification on figures.

Fig. 13. A. Pollen mass from an anther of Synangispadixis
tidwellii, showing no pollen-sac wall (about x 200). B. Epidermal cuticle isolated
from an anther, showing abundant monosulcate pollen clinging to one side (about x 500). C.
Trans-longitudinal section through portion of a male 'flower' and viewed with reflected
light, showing dark pollen masses organized in pairs (P) within each anther and separated
by septa (s); the walls of adjacent anthers separated by thin cracks or lines (small
arrows); a ventral suture to one anther is visible at lower left (open arrow); see text
for further description. D-E. Pollen from S. tidwellii anthers, showing a
monosulcate aperture and a faint intragranular exine structure. F. Cyclotriletes
margaritatus (Carnian), which is identical to spores recovered in situ from
osmundaceous fertile spikes associated with Cladophlebis macrophylla fronds and
rhizomes at the Sanmiguelia locality.

Synangispadixis microsporophylls are variable in shape, ranging
from lunate to tear-drop to narrow-elongate (Figs 10a-b; 11d-f; 12a, 12c-d). They range in
length (i.e. tip to base) from 230 to 525 microns, and in height from 170 to 407 microns.
Their size is undoubtedly reduced from that in life due to compression and shrinkage
during coalification. Most are longer (tip to base) than tall (Fig. 11e-t), but some are
taller than long (Fig.10b). Regardless of shape they all have a pronounced thickening of
cells (referred to here as the anther cap) bordering a median suture, which extends from
the apex across to the opposite side of the anther, where it seems to disappear as the
anther cap terminates. Some specimens indicate that the suture continues to near the base
of the anther (Figs. 11f; 12d; 13c). The interpretation by Cornet (1986) that the
microsporophylls had two wall layers (i.e. epidermal and endothecial) was based on the
preservation of a thick-walled cell layer surrounding the pollen masses and tapetum, and a
thin outer layer with wrinkled cuticle (Fig. 11d, 11e). An epidermal cuticle was
originally not verified because of poor preservation, but is verified here from the
maceration of anthers belonging to the specimen in Figure 11c. Psilate monosulcate pollen
was found abundantly clinging to one side of epidermal cuticles from this specimen (Fig.
13b), and is identical to that observed within the pollen chambers (Fig. 12b) or isolated
from them (Fig. 13d-e).

The paired nature of the pollen sacs, their separation by a septum that
disappeared with pollen maturity, and the lack of a true pollen sac wall were three
aspects of Synangispadixis anthers strongly stressed by Cornet (1986).
He gives several illustrations or drawings of anthers that purportedly show a septum
separating two pollen masses, but no clearer documentation of this condition can be
presented than sections through anthers. Figure 13c shows a portion of a male 'flower'
that was embedded in plastic, sectioned, and polished for reflected light study. The
position and orientation of the floral axis is indicated, and the section cuts anthers
trans-longitudinally progressively higher from lower left to upper right. The ability of
this section to traverse so many anthers in a sequential fashion indicates that they were
borne in an orderly fashion (i.e. in rows). The pollen 'sacs' (P) appear as narrow
elongate pollen masses with tapering ends, while the light reflecting ground mass
represents anther wall material. The pollen masses are each composed of hundreds of
compressed pollen grains (Fig. 13a, 13c) and occur in distinctive pairs (arrows) separated
by septa (s). An isolated pollen mass is shown in Figure 13a for comparison. No
morphologically distinct pollen sac wall or cuticle can be distinguished in most
specimens. Pollen and cuticle preparations of anthers sometimes show a discontinuous
cuticle preserved on the outside of parts of some pollen masses, suggesting the possible
presence of a vestigial or incomplete pollen sac wall. The disappearance of the septum
basally brings the pollen masses together (Fig. 13c, lower left), a condition noted by Cornet (1986: Fig.
4b). The appressed boundaries of individual anthers can be followed as faint dark
lines (Fig. 13c, small arrows), while the 'ventral' suture dividing the anther into two
symmetrical halves can be recognized near the base of one anther (Fig. 13c, open arrow).
No known fossil or recent gymnosperm possesses this type of microsporophyll construction,
and the additional paired condition of the anthers makes comparison with angiosperms the
only reasonable choice.

General discussion

A special origin for a pollen tube transmission tissue rarely has been
addressed in theories of carpel evolution in angiosperms (Cornet, 1986), and it is
generally assumed to have evolved from carpellary (i.e. leaf) tissue when the 'need' arose
(cf. Bailey and Swamy, 1951). The varying distribution of transmission tissue within the
angiosperms relative to differences in ovule and stigma position, and its integrity even
when reduced to a single cell layer of the ovary wall (e.g. Welk et al., 1965)
suggest that it is a specialized organ requiring an individual or separate origin. The
similarity in size, shape, and form of the Axelrodia middle-layer to sterile
interseminal scales in the gnetalean-like ovuliferous 'flower' (Fig. 7d) suggests that
they may be homologues. By homology the transmission tissue of angiosperms would also be
derived from highly modified interseminal scales.

Doyle and Donoghue (1986, 1987a, b) and Crane (1985) provide cladistic
evidence that the Bennettitales and Gnetales are sister groups of angiosperms, making a
search for organ and character homologies with angiosperms a logical consequence. Harris
(1932) and Crane (1985) interpret bennettitalean sterile interseminal scales as having
developed from ovule primordia, making them equal to ovules but without nucellus and egg.
Such an origin of transmission tissue from modified ovular integument would mean that the
pollen tube in angiosperms could be following ovule-derived organs from stigma to
micropyle (cf. Hill and Lord, 1987; Mulcahy and Mulcahy, 1987; Murdy and Carter, 1987).
Such an origin would also mean that the expression of gametophytic self-incompatibility in
the style, placenta, integuments, and micropyle (Zavada, 1984; Zavada and Taylor, 1986) is
in reality different organ responses of the same developmental system. Synergid
degeneration is known to be induced by pollination well before pollen tubes enter the
ovary in some angiosperms (Mulcahy and Mulcahy, 1987), indicating a communication between
stigma and embryo sac that could be accomplished only by a closed (i.e. unified) organ
system. Consequently, if angiosperm transmission tissue is derived from homologues of
bennettitalean interseminal scales, it would represent a further specialization of the
ovulary system rather than a transfer of function to a leaf-derived organ with no 'prior
experience'.

The presence of a middle layer with transmission tissue characteristics,
which extends from an apical stigma to subbasal ovules in the Axelrodia carpel
(Figs 9a-b; 6d, 6g) supports the importance of a unified self-incompatibility system in
the evolution of angiospermy (Zavada, 1984; Zavada and Taylor, 1986), and suggests that
carpel closure around unitegmic ovules, by itself, probably would not lead to angiospermy
(a number of fossil and recent gymnosperms, such as Glossopteris, Caytonia, Hirmeriella
and Araucaria, completely enclose their ovules with bract- or leaf-derived
organs without developing a system like that of angiosperms; cf. Doyle and Donoghue,
1986). Ironically, carpel closure, considered by most botanists as the hallmark of
angiospermy, may not be the cause of angiospermy (Zavada, 1984), because an intervening
organ (i.e. interseminal scales) may have enclosed and shielded the ovules as in the
Bennettitales when the carpel was still open (compare Fig. 7b and 7d). A massive type of
transmission tissue in the Chloranthaceae that surrounds a solitary ovule and projects
above the carpel through a short stylar canal to form a separate stigma in Hedyosmum (most
obvious), Ascarina, Sarcandra, and Chloranthus (least obvious: Endress,
1987a) supports an early origin of that organ system. Complete closure of the Axelrodia
carpel may have occurred as a secondary and additional control to reduce selfing (and
flower abortion) by physically limiting the area of pollen germination, thereby increasing
the chances for biotic cross-pollination with compatible pollen (Zavada, 1984, and
references therein).

The bitegmic ovule is considered basic for angiosperms, while the
unitegmic condition of some angiosperms is interpreted as derived (Crane, 1985; Doyle and
Donoghue, 1986). The second or outer integument is not homologized with any pre-existing
organ, and is considered to have evolved de novo in angiosperms (Doyle and
Donoghue, 1986). The evolution of a transmission tissue carrying specific types of
glandular cells that form a chemical pathway from stigma to micropyle may have reequired
the evolution of a second integument with similar cellular (i.e. transmission-diffusion)
properties as the transmission tissue in order for the ovule to assess male compatibility
remotely (cf. Zavada, 1984; Zavada and Taylor, 1986). The second integument of angiosperms
could be an outgrowth of transmission tissue, serving to maintain a unified organ system.
Such an origin is indicated by its subepidermal or subovule origin (Eames, 1961), although
the same evidence could be used to support an origin from surrounding interseminal scales
(examine the morphology of the robust axial transmission tissue, obturator,
orthotropous-ovule system in Anthurium [Araceae] for an example showing possible
outgrowth).

Why paired pollen sacs are basic to angiosperm anthers and why the
septum in angiosperms degenerates near anthesis are questions that bear directly on the
origin of the angiosperm anther. Synangispadixis may provide some clues to answer
these questions once correct homologies are made between angiosperm, gnetalean, and
bennettitalean microsporophylls. The bivalved microsporophyll with a central cluster of
free pollen sacs may be basic for the Gnetales (cf. Cornet, 1987a), even though later
reduction may account for the absence of paired bracts in Welwitschia. The basic
construction of bennettitalean microsporophylls is similar to that of Synangispadixis, except
that more than two pollen sacs are fused to the adaxial surfaces of paired bracts and the
bracts are not folded to enclose the sacs (Crane, 1985). In Synangispadixis space
limitation and bilateral symmetry created by folding or conduplication of the bract would
necessitate the reduction of median pollen sacs, raising the possibility that the
septum is derived from modified sporogenous tissue and represents all that remains of the
reduced sacs. Both the pollen sac 'wall' (i.e. tapetum) and septum degenerated with pollen
maturity (Cornet,
1986), suggesting that they are derived from homologous organs. The absence of a
true pollen sac waIl (as contrasted with the sporangium or anther wall) is considered by
Eames (1961: p. 127) to be 'an important angiosperm character, one that will play a major
part in the determination of the ancestry of angiosperms'.

Carpel and ovule ontogeny as indicators of angiospermy

The possession of a megasporophyll that morphologically and anatomically
resembles a closed angiosperm carpel is the first major test of angiospermous affinity,
but it tells us little about how the reproduction system functioned. A pollen-tube
transmission tissue interconnecting ovules with stigma is an angiosperm character,
suggesting male assessment by the female, but it tells us nothing about the gametophyte.
Indirect evidence of nutrient rewards for insects by the presence of glands, and direct
evidence of actual insect visitation in the form of bite marks and trails of selective
anther debris on the carpel are important for understanding pollination biology, but are
not evidence for angiospermy. The two sister groups of angiosperms, the Gnetales and
Bennettitales, are either known to be or suspected of having been visited by and
effectively pollinated by insects (Bino et al., 1984; Crepet and Friis, 1987).
Thus, one of the most important aspects about Sanmiguelia reproduction - whether
fertilization occurred before the ovule underwent significant development - must be
documented either directly by an embryo at an early stage of ovule development or
indirectly by carpel and ovule ontogeny.

Fig. 14. Graph of carpel and ovule/seed growth for Sanmiguelia
lewisii (Axelrodia) based on megasporophyll (carpel) length versus two-dimensional
area: ovule/seed size or two-dimensional area is plotted on the ordinate under the points
representing the carpels to which they belong; the curves were drawn by eye. Note the lack
of ovule development below a certain minimal carpel size and length (14 mm), followed by
the exponential growth of seeds to fill the ovary. Arrow marks estimated time of
fertilization.

Cornet (1986) graphed carpel length against two-dimensional area and
compared the resulting curve with the growth of enclosed ovules and dispersed seeds (Fig.
14). Difficulty in recognizing ovules in Axelrodia carpels smaller than 14 rnm in
length, and their rapid (i.e. exponential) growth to fill the ovary in larger carpels
suggested to him an angiospermous type of reproductive system. Furthermore, the morphology
of embryo casts within dispersed seeds suggested that fertilization occurred before ovule
development as in angiosperms. This interpretation, however, was limited by a lack
of comparative data.

Carpel or megasporophyll and ovule/seed development were measured and
plotted for three extant angiosperm species and one conifer. The resulting graphs for Magnolia
grandiflora and M. virginiana (Fig. 15), Serelloa repens (Fig. 16) and Thuja
orientalis (Fig. 17) compare carpel or cone length to weight measurement instead
of two-dimensional size. This difference creates graphs that are not directly comparable
with the graph for S. lewisii, but since two-dimensional compressions of originally
hollow structures with thin walls expand when compressed, they are close to proportional
to original size (i.e. surface area). The surface area of a hollow spheroid will increase
as the spheroid increases in size, but its mass will not increase as rapidly as for a
solid spheroid. As the thickness of the spheroid wall decreases, the change in mass will
produce a curve that approaches the shape of the curve for change in surface area. That is
probably why the graphs for Sanmiguelia and the angiosperms (particularly Magnolia)
so closely resemble one another. Since the objective of these graphs is to document a
delay in ovule development as in angiosperms, the data can be compared.

Fig. 15. Graph of carpel and ovule/seed growth for Magnolia
grandiflora and M. virginiana (Magnoliaceae) based on carpel length versus
weight in milligrams; ovule/seed weight is plotted on the ordinate under the points
representing the carpels to which they belong; the curves were drawn by eye. Note the lack
of ovule development until fertilization (represented by a certain minimal carpel size),
followed by the exponential growth of seeds to fill the ovary. Arrow marks time of
fertilization.

Fig. 16. Graph of carpel and ovule/seed growth for Serenoa
repens (Arecaceae) based on carpel length versus weight in milligrams; ovule/seed
weight is plotted on the ordinate under the points representing the carpels to which they
belong; the curves were drawn by eye. Note the lack of ovule development until
fertilization (represented by a certain minimal carpel size), followed by the exponential
growth of seeds to fill thet ovary. Arrow marks time of fertilization.

Fig. 17. Graph of cone and ovule/seed growth for Thuja
orientalis based on cone length versus weight in milligrams; ovule/seed weight is
plotted on the ordinate under the points representing the cones to which they belong; the
curves were drawn by eye. Note that ovules are fertilized very early in development before
cone scales enclose them, but seed development is unlike that in angiosperms or Sanmiguelia,
because seed growth tracks the growth of the megasporophyll or cone; unfertilized or
aborted ovules remain much smaller than the fertilized ones. Arrow marks time of
fertilization.

The most significant comparisons between the angiosperms and Sanmiguelia
are the rapid elongation of carpels before an increase in breadth or weight and the
rapid or exponential growth of ovules only after a certain minimum length of carpel is
reached. These similarities contrast with the development of Thuja megasporophyIls
and ovules, which tend to track one another much more closely. Furthermore, there is no
apparent delay in ovule growth as in angiosperms and Sanmiguelia. Thuja is
pollinated very early before its cone scales grow over and conceal the ovules and their
micropyles. In addition, delayed ovule growth in Sanmiguelia is much more
pronounced than it is in Magnolia and Serenoa, which may be caused in part
by the different methods of measurement. These differences, however, do not detract from
the fact that Sanmiguelia ovules began showing rapid growth only after the carpel
reached at least 14 mm in length and about 200 sq. mm in surface area (both sides of
compression). The inflection points on carpel and ovule curves agree very closely with
those for similar events in Magnolia and Serenoa, suggesting that ovule
development did not proceed beyond a certain size unless fertilization occurred.

A delay in ovule development by itself is not necessarily evidence for
angiospermy, because the delay could be an adaptation tied to compatible pollination (as
opposed to compatible fertilization), reducing the female expenditure if an incompatible
combination resulted in flower or carpel abortion (cf. Zavada, 1984; Zavada and Taylor,
1986). Such a delay in ovule development may have preceded the evolution of double
fertilization and endosperm formation, since precocious fertilization could have had the
effect of suppressing or circumventing nucellar and archegonial development. The
development of a very large dicotyledonous embryo that filled the entire seed in Sanmiguelia
(Cornet,
1986) suggests, however, that pre-fertilization nucellar food reserve, if it formed,
did not occupy a significant volume of the ovule, otherwise it would have had an influence
on embryo shape and size. Cornet (1986) was able to show that seed shape conformed very closely
to the shape of the embryo, implying that both ovule and embryo growth were synchronous.
Such a characteristic is found only in the angiosperms, and is a strong indication that
the timing of ovule growth in Sanmiguelia was probably tied to fertilization.

Conclusions

Based on the works of Brown (1956), Tidwell et al. (1977), and Cornet (1986),
the leaves, stems, roots, growth habit and habitat of Sanmiguelia lewisii indicate
a semiaquatic woody herbaceous plant that resembled extant Veratrum californicum (the
False Hellebore of the western United States) in form and stature, but which produced a
series of clustered innovations of a few years' duration along a spreading rhizome. The
rhizomatous habit, vesselless secondary xylem of restricted development in the lower part
of the stem, and a dicotyledonous embryo (see Cornet, 1986,
for documentation) are characters shared with Sarcandra and Chloranthus (Chloranthaceae),
two of the most primitive living dicots (Carlquist, 1987). Both Sarcandra and Sanmiguelia
have vessels restricted to their roots as in some monocots and ferns (Carlquist,
1987). The monocot-like leaf morphology and leaf venation, sheathing leaf base, and
monocot-like inflorescences subtended by large spathe like vegetative leaves on a plant
that otherwise compares with primitive herbaceous dicots indicate a plant more primitive
than any living monocot or dicot.

The presence of a closed carpel with ventral suture, an
apical stigma, an ovarian organ probably adapted for pollen-tube transmission, paired
subbasal anatropous ovules with indications of two integuments, ovules that probably
developed only after fertilization, a dicotyledonous embryo with two large cotyledons, one
of which was significantly larger than the other, ovuliferous flower-like units possessing
a perianth comprised of large and specialized bracts, biloculate anthers borne in pairs
and lacking distinct pollen sac walls, anther septa that disappeared at pollen maturity,
and monosulcate pollen strongly indicate an angiospermous affinity. Clusters of female
floral subunits borne separately below large apocarpous unisexual flowers, and male
infloresences comprised solely of floral subunits that may be homologues of angiosperm
stamen indicate a plant much more primitive than any angiosperm currently described from
the Cretaceous (e.g. Retallack and Dilcher, 1981; Crane and Dilcher, 1984; Dilcher and
Crane, 1984; Dilcher and Kovach, 1986; Friis and Crepet, 1987). Consequently, Sanmiguelia
lewisii can be assigned only to the taxonomic level of Division (i.e.
Angiospermae), and preserves an intermediate stage in the evolution of the angiosperm
flower.

The early to middle Carnian Crinopolles Group of monocot-like pollen
from the Richmond basin, Virginia (Cornet, 1989) demonstrates that numerous palynological
characters thought to be typical and diagnostic of monocots (Doyle, 1913; Walker and
Walker, 1984) appeared very early in the Mesozoic, possibly near the time of angiosperm
origin (Crane, 1985; Doyle and Donoghue, 1986: p. 384, 1987b: p. 37). The presence of Sanmiguelia
in the Carnian of North America supports Burger's (1981) contention that monocot
characters played a significant role in early angiosperm morphology. Although there is
still no clear evidence as to why angiosperms did not radiate in the Triassic or Jurassic,
the fact that they did not can no longer be used as reasonable evidence for a later origin
(Crane, 1988). Doyle and Donoghue (1987b: p. 41) suggest that carpel closure may be
the reason for the radiation of angiosperms in the Cretaceous, but that cannot be the case
if Sanmiguelia is an angiosperm or directly related to them. If double
fertilization had not (yet) evolved in Sanmiguelia, carpel morphology and ovule
development at least suggest the presence of an early self-incompatibilty system. The
reason for a delayed radiation may therefore be more complex, having been the result of
several factors including the evolution of deciduous leaves with petioles and
hermaphroditic (i.e perfect) floral morphology; co-evolution with pollinators and the
availability of numerous faithful pollinators; increased number of niches due to the
extinctions of certain groups of gymnosperms; changes in climate, sea level, and available
land masses; and a variety of factors associated with pollination, seed dispersal, and
herbivory (Taylor, 1988). Perhaps, like Paleocene mammals, angiosperms had to wait for the
right combination of changes in the Cretaceous (e.g. Bakker, 1978, 1986) before a
sustained radiation could occur.

Acknowledgements

This paper is dedicated to my wife, Bonnie Lee Cornet, for her
determined and heroic struggle against the ravages of a merciless cancer. The author is
grateful to the Department of Geological Sciences, Columbia University and Dr G. Bayliss,
President of GeoChem Labs. Inc., Houston, TX for providing laboratory space and equipment,
and for the use of reflectance and light microscopes. He acknowledges US National Science
Foundation Grant BSR 87-17707 to P.E. Olsen for support to the author. He thanks W.A.
McHale (President of Accumin Analysis Inc., Houston, TX) and the former Gulf Research
& Development Co. (now Chevron) for SEM work; Dr P.A. Murry and E.B. Cornet for field
assistance at the Sunday Canyon locality; Dr J. Morgan (retired, Exxon), Dr C. Sancetta
(Lamont), and Dr L.E. Stover (Exxon Co., USA) for the use of their microscopes; and Drs
P.R. Crane, P .E. Olsen, D. Peteet, A. Raymond and C. Sancetta for their helpful comments,
advice, and suggested improvements for this manuscript.